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To be completed by the Secretariat:

Document No.: WG-EMM-13/28

Date submitted: 16 June 2013

Original Language: English

To be completed by the author:

Meeting: WG-EMM-13

Agenda Item No(s): 2.1.4

Title A Critical Re-examination of the Evidence for a Possible Dependence of

Weddell Seals (Leptonychotes weddellii) on Antarctic toothfish

(Dissostichus mawsoni) in the Ross Sea, Antarctica

Author(s) R. Eisert1,2

, M.H. Pinkerton3, S.D. Newsome

4, O.T. Oftedal

2

Address(s) 1 Gateway Antarctica, University of Canterbury, New Zealand

E-mail: regina.eisert@canterbury.ac.nz 2 Smithsonian Environmental Research Center, USA

E-mail: oftedalo@si.edu 3 National Institute of Water and Atmospheric Research Ltd (NIWA),

Wellington, New Zealand.

E-mail: m.pinkerton@niwa.co.nz 4 University of New Mexico, Albuquerque, USA

E-mail: newsome@unm.edu

Name and email address of person submitting paper: ben.sharp@mpi.govt.nz

Published or accepted for publication elsewhere? Yes No

If published or in press, give details:

To be considered for publication in CCAMLR Science?1 Yes No

1 By indicating that the paper is to be considered for publication in CCAMLR Science, the authors have agreed that the paper can

be considered by the Editorial Board of the journal and that, if the paper is accepted for peer review, it is the responsibility of

the authors to ensure that permission to publish data and cite unpublished working group papers has been received.

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Abstract

There is presently debate over the degree to which the fishery for Antarctic toothfish (Dissostichus

mawsoni; ‘toothfish’) in the Ross Sea may affect the ecological viability of top predators such as

Weddell seals (Leptonychotes weddellii), but available evidence remains inconclusive as a result of

both methodological limitations and knowledge gaps. We present new stable isotope data on

Weddell seal prey, consider the assumptions underlying application of stable isotope methodology to

Weddell seals, and estimate the potential contribution of toothfish to the diet of Weddell seals using

an isotope mixing model. As a new approach, we also estimate Weddell seal food requirements by

considering nutritional quality of potential prey species including toothfish in the context of updated

estimates of Weddell seal energy requirements. The energy density of potential prey items (fish and

invertebrates) covers a four-fold range. Nutritional analysis of Ross Sea prey suggests that toothfish

may represent a unique high-energy food resource for Weddell seals that possibly cannot be

adequately replaced by other prey, in particular during periods of high energy demand such as late-

stage lactation and the post-breeding recovery of body weight and condition. The assumed

dominance of Antarctic silverfish (Pleuragramma antarcticum) in Weddell seal diets should be re-

examined given the known biases of methods used to derive diet estimates. While large (>30 g)

silverfish occurring at high densities are a valuable nutritional resource, smaller size classes are

unlikely to be adequate to meet the estimated energy requirements of adult Weddell seals. Our

ability to conclusively determine possible dependence of Weddell seal populations on toothfish, and

hence possible impacts of toothfish removal by fisheries, is primarily hindered by (a) insufficient

information on Weddell seal diet, due to inadequate temporal coverage and biased methodology,

and (b) uncertainty regarding Weddell seal abundance and spatial foraging patterns in the Ross Sea

region.

This paper is presented for consideration by CCAMLR and may contain unpublished data, analyses,

and/or conclusions subject to change. Data in this paper shall not be cited or used for purposes

other than the work of the CAMLR Commission, Scientific Committee or their subsidiary bodies

without the permission of the originators and/or owners of the data.

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I. INTRODUCTION

Marine mammals are potentially affected by fisheries both directly, e.g., through bycatch mortality,

and indirectly, through a reduction of their prey biomass. Indirect impacts on marine mammals may

be significant but are much more difficult to quantify than direct effects (Moore 2012).

There is presently debate over the degree to which the fishery for Antarctic toothfish (Dissostichus

mawsoni; ‘toothfish’) in the Ross Sea may exert indirect trophic impacts on top predators such as

Weddell seals (Leptonychotes weddellii; e.g., Ponganis & Stockard 2007; Ainley et al. 2009; Ainley &

Siniff 2009). Weddell seals breed in summer in the vicinity of McMurdo Sound (Fig. 1) and

elsewhere in the Ross Sea region (Stirling 1969a, 1971a). As reviewed by Pinkerton et al. (2008), the

most likely potential impact of the fishery on Weddell seals in the Ross Sea is a reduction in prey

availability arising from depletion of toothfish by the fishery, but the available body of knowledge is

insufficient to (a) quantify toothfish intake by Weddell seals (of any subpopulation or at any time of

year), and hence (b) to assess the risk of impacts of the fishery on Weddell seals, and possibly other

species, in the Ross Sea. There are marked, unresolved discrepancies in existing diet information

regarding toothfish consumption by Weddell seals: Direct methods (observation, stomach contents,

photography) support significant predation on toothfish by Weddell seals, whereas indirect methods

(stable isotope analysis, scat hard part analysis) appear to point to Antarctic silverfish (Pleuragramma

antarcticum)and cryopelagic fish such as bald notothen (Pagothenia borchgrevinki) as the principal

food resource of Weddell seals in McMurdo Sound.

In this paper, we critically re-examine available evidence regarding Weddell seal diet and the possible

importance of toothfish for Weddell seals. Stable isotope analysis shows great promise for

determining long-term diet. We present new stable isotope data on prey, discuss several key

assumptions underlying application of stable isotope methodology to Weddell seals, and estimate

the potential contribution of toothfish to the diet of Weddell seals using an isotope mixing model. As

a new approach, we also estimate Weddell seal food requirements by considering nutritional quality

of potential prey species in the context of updated estimates of Weddell seal energy requirements.

The energy density of potential prey items (fish and invertebrates) covers a four-fold range, and the

estimated energy requirements of Weddell seals vary greatly with season and among subpopulations

(breeding vs. non-breeding adults, growing subadults). These factors have a direct effect on the

mass (and possibly type) of prey consumed. Combining estimates of possible toothfish consumption

derived from stable isotope analysis and energetic considerations, we estimate plausible rates of

toothfish consumption by Weddell seals and compare them to estimates of Antarctic toothfish

production and mortality in the vicinity of McMurdo Sound.

II. Weddell Seal Biology and Life History

Weddell seals (Leptonychotes weddellii) are one of five Antarctic pinniped species. Due to their

unique ability to dive under closed sea ice, Weddell seals are the only marine mammal able to exploit

continental shelf habitats around the Antarctic continent that are covered by contiguous sea ice for a

large proportion of the year. Weddell seals occur in large numbers on the circumpolar fast ice, and

offshore in the pack ice zone north to the Antarctic Convergence (Kooyman 1981). The

northernmost breeding limit of Weddell seals is South Georgia (54° 30' S; Vaughan 1968). Weddell

seals are distributed throughout the Ross Sea, forming large breeding colonies of up to several

hundred animals along the coasts of Victoria Land and Ross Island (Ainley 1985; Testa & Siniff 1987).

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Figure 1. Subareas 88.1, 88.2A and 88.2B showing the McMurdo Sound region (red).

Weddell seals breeding in the southern Ross Sea have been extensively studied. In McMurdo Sound,

Weddell seals were first studied by Wilson in 1902-04 (Wilson 1907), and later establishment of

American and New Zealand research stations has resulted in almost continuous research activity

directed towards local breeding colonies (e.g., Smith 1965; Stirling 1967, 1968, 1969b, a, 1971b,

1974; Testa 1987; Testa et al. 1989; Burns & Castellini 1996; Schreer et al. 1996; Burns et al. 1998;

Testa & Scotton 1999; Stewart et al. 2003; Cameron & Siniff 2004; Proffitt et al. 2009; LaRue et al.

2011; Eisert et al. 2013a). An intensive study of the population ecology of a breeding population of

Weddell seals in the Erebus Bay region of eastern McMurdo Sound, started during the 1960s by the

New Zealand Antarctic Programme and continued by American researchers, continues to the present

and is the longest-running study of any wild mammal (e.g. Stirling 1967; Rotella et al. 2009). Over

the course of this study, over 17,000 animals have been tagged, with emphasis on maintaining and

enhancing annual demographic data through the use of mark-recapture techniques (Rotella et al.

2009). In contrast to the wealth of information collected on demographics, few studies have

targeted the nutritional ecology of the Weddell seal, and there is a paucity of information not just on

diet, but on the energetic and nutritional requirements of all seal age classes.

In the austral spring, adult Weddell seals congregate in breeding colonies to give birth, raise their

young, and mate. Colonies tend to form near tidal cracks in fast ice in traditional locations, often at

considerable distance from open water. Once female Weddell seals are of breeding age, they show a

high degree of philopatry for colonies (Hastings et al. 1999). Mean parturition and weaning dates

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depend on colony location and occur earlier in the northern part of the range (Mansfield 1958;

Vaughan 1968). In McMurdo Sound (Fig. 1), one of the most southerly breeding locations, pupping

starts around October 12, with peak pupping occurring during the last week of October. Pregnant

females arrive at colony sites a few days before giving birth. Non-breeding adults are excluded from

the colonies by aggressive behaviour of adult males and females with pups (Stirling 1969b). Weddell

seal pups are born at an advanced stage of maturity (Eisert et al. 2013b), start diving in their second

week of life, and are weaned after nursing for only 5 to 8 weeks (Eisert et al. 2013a). Lactating

females fast initially before the majority starts to feed near the breeding colonies at two to four

weeks postpartum (Hindell et al. 2002; Eisert et al. 2005). Adult males defend underwater territories

(= maritories) associated with fast-ice colonies and compete for access to females, which come into

oestrus towards the end of lactation (late November to mid-December; Hill 1987). Weddell seals

have an extreme ‘capital breeding strategy’, i.e., they catabolise a large proportion of their body

mass (BM) to support the energetic demands of reproduction during the austral spring and summer

(Eisert & Oftedal 2009). Female Weddell seals may lose ≥40% of their postpartum BM during

lactation (Eisert & Oftedal 2009), and sexually active males also sustain high rates of mass loss

(Bartsh et al. 1992; Table 4). Because lactating Weddell seals have one of the largest mass losses of

any pinniped, it was previously thought that food intake during lactation was opportunistic and did

not contribute significantly to energy requirements (Oftedal 2000; Eisert & Oftedal 2009). However,

preliminary data on the energetics of lactation and food consumption in lactating Weddell seals

indicate that food intake is significant and possibly essential for successful completion of lactation

(Eisert, Oftedal et al., unpublished data; Oftedal & Eisert 2010). There is evidence that weaning mass

has a direct effect on pup survival in Weddell seals, indicating that any factors that decrease lactation

performance (such as inadequate prey availability or quality) may have a detrimental effect on

offspring survival (Hadley et al. 2008; Proffitt et al. 2008).

After the six-week lactation period (late Oct-early Dec), adult Weddell seals move short distances

(~2-10 km) away from breeding colonies and aggregate in other areas of sea ice; for example, many

Weddell seals in the Erebus Bay region move to haul-out areas near Turtle Rock and the pressure

ridges near Scott Base, where they remain for the annual moult (Jan-Feb; Smith 1965). The annual

moult takes place shortly after the breeding season (late December-January) and is likely to

represent an additional, energetically demanding period for Weddell seals (Boily 1996; Table 4).

Weddell seals have delayed implantation (Smith 1966), i.e., there is a variable delay between

fertilisation and implantation of the blastocyst. This mechanism serves to synchronise parturition

dates among individuals of a population to take advantage of the narrow window of optimal ice and

climatic conditions during the short Antarctic spring and summer. Body condition is known to have a

decisive influence on whether blastocyst implantation takes place at all in other carnivorans

(Lindenfors et al. 2003), and successful implantation and subsequent foetal development in Weddell

seals may be contingent on the ability to recover the massive weight loss incurred during the

preceding lactation period. If this is the case, it would imply not only a strong dependency of seals

on local, high-quality prey during the immediate post-breeding season, but it also means that a

decrease in prey availability or quality at this time may have a disproportionate detrimental impact

on this species. There is very little information on feeding activity in Weddell seals during the period

from December to February, partly because access on unstable sea ice may be difficult, and because

no instruments can be attached to seals to monitor their behaviour during the moult. Late lactation

and post-breeding are periods when seals would be expected to benefit greatly from feeding on

abundant and/or high-quality prey to replace lost body stores.

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The spatial distribution of Weddell seals between March – October is not certain. Some individuals

remain year round in the fast ice at latitudes as high as 78°S in McMurdo Sound, whereas others,

particularly newly weaned and subadult animals, appear to spend the winter in the pack ice to the

north of the Ross Sea (Stewart et al. 2003). Ice conditions, the availability of prey, and the

abundance of predators such as leopard seals and killer whales likely determine where adults and

young go when they disperse from the breeding colonies (Testa 1994). Tagging experiments show

that some pups born in McMurdo Sound return there within a year, while others stay more than

400 km distant for a number of years (Burns et al. 1999). Fewer than 15% of pups born in the Erebus

Bay area of McMurdo Sound have been observed recruiting into the breeding population near their

birth locality by six years of age (Testa 1987; Hastings et al. 1999). The low return rate may be

because pups suffer high mortalities in their first few years of life, because pups recruit into other

colonies, and/or because studies are not long enough to observe pups returning to their natal areas

(Burns et al. 1999). Satellite tracking of adult females from breeding colonies in McMurdo Sound

showed that most remained in the northern part of the Sound during winter, although some

travelled as far as 500 km north beyond the Sound (Testa 1994).

In summary, the extreme capital breeding strategy of Weddell seals indicates two periods of

potentially critical dependence on local, high-quality food resources: (1) during late lactation, if food

intake is required to allow lactating females to successfully raise their pups to a weaning weight

consistent with subsequent pup survival; and (2) during the post-breeding period, assuming that

implantation of the blastocyst and early foetal development depend on the ability of females to

regain mass lost during lactation.

III. Weddell Seal Diet

Because prey consumption may exhibit both short- and long-term variability, meaningful

determination of prey consumption by predators requires methods that can integrate diet

information across multiple time scales from days to months and beyond. A limitation of existing

methods of determining diet is that there is an inverse relationship between specificity and time

scale. Methods that allow determination of prey to species level and/or quantification of biomass

intake represent dietary snapshots (underwater video cameras and scat and stomach sampling),

whereas methods that integrate dietary intakes over weeks to months provide information on the

average trophic level of the diet (stable isotope analysis of predator tissues). Fatty acid analysis

appears to offer both a useful time scale as well as moderate specificity (Budge et al. 2006).

However, in the only study that has applied fatty acid analysis to Weddell seals to date, findings were

inconclusive due to difficulties of interpretation and lack of a reference data base for prey fatty acids

(Wheatley et al. 2007). The status of available knowledge on Weddell seal diet and foraging was

reviewed in a previous paper (Pinkerton et al. 2008), and there has been a recent detailed review of

diet determination in pinnipeds that examines inherent biases of existing methods (Bowen & Iverson

2012).

III.1 Evidence from Stable Isotope Analysis

Stable isotope ratios of carbon and nitrogen (δ15N, δ13C) are widely used in marine ecology and

ecophysiology to study trophic relationships and ecosystem dynamics (Newsome et al. 2010).

Ingestion and assimilation of prey results in fractionation of naturally occurring isotopes in prey due

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to metabolic processes in the predator (e.g., amino acid turnover and urea formation), and this

results in diagnostic changes in isotope abundance across trophic levels (Newsome et al. 2010).

Fig. 2 shows δ15N values for a range of megafaunal predators and fish and invertebrate prey based on

published data from (Burns et al. 1998; Bury et al. 2008; Krahn et al. 2008) and additional data on

prey from McMurdo Sound and on blood plasma collected from lactating Weddell seals (Eisert,

Newsome, Oftedal, unpubl. data). The average of reported δ15N of Weddell seals is 13.0 ‰ (Burns

et al. 1998; Zhao et al. 2004; Eisert, Newsome, Oftedal, unpubl. data). If one assumes a trophic shift

of +3.4 ‰ (Newsome et al. 2010) and a diet primarily composed of a single prey species, stable

isotope values are consistent with silverfish as the principal prey for Weddell seals; significant

consumption of toothfish by Weddell seals and Type C killer whales (Orcinus orca) appears to be

ruled out on the basis that δ15N signatures of these marine mammals are the same or slightly lower

than those of toothfish (Krahn et al. 2008; Fig. 2). Given that the two megafaunal predators with the

highest δ15N, Weddell seals and type C killer whales (Fig. 2), have δ15N on par with toothfish, this

implies that toothfish do not have any predators in the Ross Sea. This seems implausible, and

ignores the effect of isotopic mixing in predators consuming prey from a range of trophic levels, as

well as direct observations of predation on toothfish by both predators. For example, tissue of a

McMurdo octopod (Pareledone turqueti) had δ15N values higher than either toothfish or Weddell

seals (Fig. 2), even though octopods are a known prey item for Weddell seals in McMurdo Sound;

remains of Pareledone and/or related octopods were found in 14% of 36 seal stomachs (Dearborn

1965) and 10% of 290 seal stomachs collected in McMurdo Sound (Smith 1966). These discrepancies

likely derive from differences in isotopic enrichment among different tissue types, plus the effects of

diet mixing in which prey of low isotopic enrichment counterbalance prey of high enrichment.

Table 1. Maximum proportions of prey species in the diet of Weddell seals based on δ15N values as explained in the text. The values in grey indicate that the secondary constraint has been reached (diet items not to be greater than 50% of diet).

Maximal proportion in Weddell seal diet

Prey species DM PA PG TL TB

Leptonychotes weddellii 0.15 0.7 0.5 0.45 0.4

DM, Dissostichus mawsoni; PA, Pleuragramma antarcticum; PG, Psychroteuthis glacialis; TB, Trematomus bernacchii; TL, Trematomus loennbergii

We therefore employed a mixing model (IsoSource: Phillips & Gregg 2003) to determine the range of

diets of Weddell seals that is consistent with existing stable isotope data. We set the diet resolution

to 5% and the tolerance to 0.1 ‰ (Phillips & Gregg 2003). We further constrain IsoSource by

requiring that Pleuragramma antarcticum should not be less than 30% of the diet, and that

Psychroteuthis glacialis, Trematomus loennbergii and Trematomus bernacchii should each not be

more than 50% of the diet. These are termed “secondary constraints”. The primary constraints

come from the nitrogen isotope information itself. There is considerable uncertainty on the use of

δ13C to infer diet given differences in lipid extraction protocols; since we are primarily interested in

determining trophic level, we only use the nitrogen isotope and assume changes in δ15N of +3.4 ‰

per trophic level (Newsome et al. 2010). Assuming that these secondary constraints are reasonable,

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the δ15N stable isotope data are consistent with a ≤15% contribution of toothfish to the diet of adult

Weddell seals.

Figure 2: Stable isotope (δ15N) enrichment in Antarctic prey and predators. Sources of data include Burns et al. (1998), Bury et al. (2008), Krahn et al. (2008), and Eisert, Newsome, Oftedal, unpublished data. The dashed line indicates the expected trophic shift between Weddell seals and prey.

The question remains whether existing stable isotope information for Weddell seals adequately

reflects diet in McMurdo Sound. An important consideration for inferring predator diets from tissue

stable isotope patterns is the time scale of incorporation. Dietary isotopes are assimilated via tissue

turnover, which depends on the metabolic rate of the tissue and animal (MacAvoy et al. 2006, 2012).

In Weddell seals, stable isotope values have been determined in blood plasma (Burns et al. 1998). As

ca. 97% of the nitrogen in blood plasma resides in plasma proteins (Krebs 1950), changes in the

nitrogen signature of plasma are primarily determined by the turnover of plasma proteins, which

scales to the quarter power of adult BM (BM0.25) among mammals (Allison 1960; Jarnum 1975). For a

400-kg adult Weddell seal, estimated half-lives of the two dominant plasma proteins, albumin and

-globulin, are ca. 24 days for albumin and ca. 28 days for -globulin (Allison 1960). Incorporation of

a new dietary signal into plasma proteins takes 2 to 3 half-lives, corresponding to replacement of

75% to 87.5% of the resident proteins. This process would require approximately 52 to 78 days in an

adult Weddell seal, not a few days, as it sometimes assumed (e.g., (Ainley & Siniff 2009). Reported

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half-life values for δ15N in plasma proteins in captive cetaceans are ca. 20 days for bottlenose

dolphins (Tursiops truncatus, 200 kg BM) and 42 days for killer whales (Orcinus orca, ~2,000 kg BM;

Caut et al. 2011), and are in perfect agreement with predicted plasma protein half lives of 20-24 days

and 40 to 46 days for mammals weighing 200 and 2,000 kg, respectively. Burns et al. (1998)

measured δ13C and δ15N blood from pup (n = 16), yearling (n = 14), and adult (n = 12) Weddell seals at

breeding colonies in McMurdo Sound, and blood samples were taken over a number of seasons

(1992–1994). While the dates of collection are not given by Burns et al. (1998), sampling most

probably occurred sometime between mid-October (arrival of seals) and early January, as travel on

sea ice tends to be difficult after this time. Plasma samples collected during November to December

reflect the diet during September and October; to infer diet in the late lactation/post-breeding

season (late November to late December), when seals sustain very high rates of energy expenditure

and/or are recovering from massive weight loss, plasma samples would need to be collected after

the end of January. Near-annual fishing for toothfish in McMurdo Sound (1972–2011) indicates that

catch rates of toothfish from research longlines increases markedly after September (Ainley et al.

2012). Stable isotope values reported for Weddell seals captured in the pack ice of the eastern Ross

Sea between late December and early February (13.04±0.92 ‰, n = 22; Zhao et al. 2004) likely

reflect the diet of non-breeding seals foraging over deeper water (Ackley et al. 2003). It follows that

existing stable isotope information is insufficient to provide conclusive evidence either for or against

toothfish consumption by Weddell seals in McMurdo Sound, because it is likely that plasma samples

collected from Weddell seals represent dietary information during a time of year when seals have

little or no access to toothfish.

III.2 Evidence from other Methods of Diet Determination

In addition to stable isotope analysis, the bulk of evidence for Weddell seal diets has been derived

from scat hard part analysis, i.e., the recovery and identification of diagnostic prey remains (such as

sagittal otoliths, vertebrae, cephalopod beaks) from Weddell seal faeces. Scat hard part analysis is

biased in favour of prey with resistant hard parts (Bowen & Iverson 2012). Weddell seals selectively

feed on the soft tissues of toothfish so that scat hard part analysis will almost certainly fail to detect

toothfish consumption (Calhaem & Christoffel 1969; Ainley & Siniff 2009; Kim et al. 2011). This

method also provides frequency rather than mass estimates, a point particularly relevant for

assessing the dietary importance of silverfish vs. toothfish and other prey species. Silverfish otoliths

are readily detected in large numbers in Weddell seal scats (Castellini et al. 1992), and, through

confounding of frequency and mass data, this has led to the assumption that silverfish is the

predominant prey for Weddell seals. For example, Burns & Kooyman (2001) state that

“Green and Burton (1987) demonstrated that Weddell seals were even more specialized fish

consumers (99.3% diet by mass). In addition Pleuragramma antarcticum, the Antarctic

silverfish, is the primary fish prey for both predators (88.6% by numbers for penguins, 95.3%

for seals; Castellini et al., 1992; Cherel and Kooyman, 1998).”

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However, it is invalid to equate numerical dominance with biomass dominance (and incidentally

equally invalid to assume that all fish prey are silverfish). A small abundant prey item can have a high

frequency of occurrence – possibly even through secondary ingestion –, yet contribute relatively little

to the total amount of food and energy consumed. The magnitude of error introduced by confusing

data on prey number with data on prey mass has been pointed out by (Ainley & Siniff 2009). To

illustrate, if a Weddell seal consumed one toothfish (18 kg BM, ingested portion 10.8 kg) and

100 silverfish of 31 g each, the resulting ratios would be 3.5: 1 (toothfish: silverfish) for ingested

biomass. The error is exacerbated further by the fact that seals can obtain considerably more energy

(metabolisable energy, ME; see section below) from toothfish than from silverfish (Table 3). When

relative prey intakes are considered in terms of energy (ME), the ratio becomes 5.4: 1 in favour of

toothfish, while scat analysis would show only silverfish consumption.

Further direct evidence of toothfish availability to Weddell seals comes from underwater video

recorded using cameras attached to free-ranging Weddell seals in McMurdo Sound. In one study,

seals encountered 336 silverfish in 58 dives and toothfish 26 times in 14 dives (Fuiman et al. 2002).

The silverfish had a reported total length (TL) of 20 to 25 cm, corresponding to a standard length (SL)

of 17.6 to 22 cm (Azzali et al. 2010) and a mean BM of ca. 65 g (O'Driscoll et al. 2011), which is larger

than the reported modal SL and mass of adult silverfish in the Ross Sea (SL 17 cm, BM 40 g; O’Driscoll

et al. 2011). If we consider only the 13 encounters between seals and toothfish reported by Fuiman

et al. (2002) that are known to be different fish, and further assume that seals ate the toothfish

following only one in ten encounters, then the energy intake from the two prey types would be

9.4 MJ ME per dive for toothfish vs. 3.9 MJ ME per dive for silverfish. Davis et al. (1999) reported

that in addition to encounters with silverfish and toothfish, seals equipped with underwater video

cameras flushed bald notothens (Pagothenia borchgrevinki) out of crevices in the under-ice surface.

While direct observations of stomach contents (Dearborn 1965; Green & Burton 1987) from

McMurdo Sound indicate that fish remains occur in close to 100% of sampled seals, it is not true that

silverfish is the only or even the dominant fish species taken by Weddell seals. In Dearborn (1965),

fish remains were present in 35 of 36 seal stomachs, but silverfish were positively identified in only

4 samples (11%); by comparison, fishes of the genus Trematomus occurred in 14 stomachs (39%).

Smith (1966) examined 290 stomachs of Weddell seals collected in McMurdo Sound and reported

that the results “were similar to those of Dearborn”, and “in the Cape Armitage region [near Scott

Base in McMurdo Sound], channichthyids were the predominant fish taken by Weddell seals”. There

is also evidence that cryopelagic fish (species living in or near the under-ice surface) may be

important prey items for Weddell seals. Cryopelagic fish in the Ross Sea include P. borchgrevinki,

P. brachyosoma, and Trematomus newnesi (Andriashev 1970; Gon & Heemstra 1990). In addition to

camera observations reported by Davis et al. (1999) (above), P. borchgrevinki have been found

cached in ice holes (Kim et al. 2005) and as otoliths in seal scat (Castellini et al. 1992). Trematomus

newnesi has been reported as prey of Weddell seals near Mawson Station, 67°36' S 62°52' E (Lake et

al. 2003); T. newnesi occurs in the Ross Sea and fishes of the genus Trematomus are frequently eaten

by Weddell seals in McMurdo Sound, although they are rarely identified to species level (Dearborn

1965; Burns et al. 1998; Table 2). Consumption of T. newnesi by Weddell seals is therefore plausible.

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Table 2: Reported prey species of Weddell seals in the Ross Sea region. Identification refers to the lowest taxonomic level reported in the original source. For prey items reported in multiple sources , only the most direct method is given in order of priority. Taxonomy follows ITIS (www.itis.gov). MCM, McMurdo Sound.

Category Order or superorder Family Prey Identification ID Level Method Area Reference

Fish Perciformes Bathydraconidae -- family stomach contents MCM Dearborn 1965 Gymnodraco (acuticeps)* genus stomach contents MCM Wilson 1907

Channichthyidae -- family stomach contents MCM Dearborn 1965

Cryodraco antarcticus species stomach contents MCM Smith 1966

Pagetopsis macropterus species stomach contents MCM Smith 1966

Nototheniidae Notothenia genus stomach contents MCM Wilson 1907

Dissostichus mawsoni species eye witness MCM Calhaem & Christoffel 1969

Pagothenia borchgrevinki species underwater camera MCM Davis et al. 1999

Pleuragramma antarcticum species stomach contents MCM Dearborn 1965

Trematomus spp genus stomach contents MCM Wilson 1907, Dearborn 1965

Crustacean Euphausiacea Euphausiidae Euphausia superba† species stomach contents Bay of Whales Lindsey 1937

Decapoda Hippolytidae Chorismus antarcticus species stomach contents MCM Dearborn 1965

Mysida Mysidae Antarctomysis ohlinii species stomach contents MCM Dearborn 1965

Isopoda Cirolanidae Cirolana spp. genus stomach contents MCM Dearborn 1965

Amphipoda Eusiridae Eusirus microps species stomach contents MCM Dearborn 1965

Cephalopod -- -- "cephalopods" class stomach contents MCM Testa et al. 1985

Octopoda Octopodidae Pareledone charcoti‡ species stomach contents MCM Smith 1966

Decabrachia Brachioteuthidae Brachioteuthis picta species scat analysis MCM Burns et al. 1998

Gonatidae Gonatus antarcticus species scat analysis MCM Burns et al. 1998

Histioteuthidae Histiotheutid spp. genus scat analysis MCM Burns et al. 1998

Mastigoteuthidae Magistoteuthiid spp genus scat analysis MCM Burns et al. 1998

Onychoteuthidae Kondakovia longimana species scat analysis MCM Burns et al. 1998

Psychroteuthidae Psychroteuthis glacialis species eye witness MCM Kooyman et al. 1988

* identified simply as “Gymnodraco” in the source but there is only one species in this genus; †found in the stomach of a weaned pup; ‡this may in fact be

Pareledone turqueti (Oftedal, Vecchione, Eisert et al., unpubl. data)

12

Table 3: Energy content of fish and invertebrate prey species calculated from data in Lenky et al. (2012) and additional sources as indicated. Metabolisable energy (ME) content was calculated from proximate composition using values of 38.1 kJ.g-1 for lipid and 16.74 kJ.g-1 for crude protein (CP); gross energy (GE) was measured directly or calculated using equivalents of 39.3 kJ.g-1 for lipid and 23.6 kJ.g-1 for CP. GE values that were calculated rather than measured are indicated by an asterisk (*). ME: GE ratios of less than 75% are shown in bold type. BM, body mass; DM, dry matter; SL, standard length

SL BM H2O DM lipid CP ash lipid GE ME ME/GE

Species [cm] [g] [%WM] [%WM] [%WM] [%WM] [%WM] [%DM] [kJ.g-1] [kJ.g-1] [%]

Pareledone spp. (octopus)§ 28.4 57.0 84.3 15.7 1.3 10.8 1.8 8.3 3.1 2.3 75.3

Euphausia superba (krill)*‡ a n/a n/r 80.1 19.95 3.5 10.5 3.5 17.5 4.3 3.0 68.9

Bathylagus antarcticus 15.1 38.6 87.3 12.7 2.8 8.2 1.8 21.9 3.1 3.1 77.5

Electrona antarctica† 8.1 7.4 69.6 30.4 15.6 12.4 2.5 51.4 9.2 5.5 59.5

Electrona carlsbergi 7.2 5.5 73.9 26.1 7.8 14.9 3.0 29.8 6.7 5.5 81.4

Gymnoscopelus braueri† 10.1 9.0 68.5 31.5 15.6 13.8 2.7 49.4 9.7 5.7 58.6

Gymnoscopelus nicholsi 14.9 37.0 64.9 35.1 18.0 14.7 2.3 51.2 10.7 9.3 87.1

Dissostichus mawsoni (muscle) -- -- 68.7 31.3 15.8 15.4 0.9 50.4 9.9 8.6 86.8

Lepidonotothen squamifrons 22.4 291.0 81.3 18.7 2.7 13.3 2.9 14.2 4.6 3.2 70.6

Pagothenia borchgrevinki 21.2 132.8 77.0 23.0 5.3 15.2 2.4 22.9 5.7 4.5 80.1

Pleuragramma antarcticum juvenile*b 8.0 2.9 88.0 12.0 2.3 7.7 1.4 19.2 2.7 2.2 79.6

Pleuragramma antarcticum adult 13.4 23.7 82.2 17.8 7.4 8.7 1.5 41.6 5.0 4.3 86.1

Pleuragramma antarcticum adult*b 15.5 31.0 78.3 21.7 10.2 9.8 1.7 47.0 6.3 5.5 87.4

Trematomus bernacchii 16.4 75.9 76.6 23.4 4.2 16.1 3.0 17.9 5.5 4.3 77.6

Trematomus eulepidotus 19.6 121.8 75.6 24.4 4.6 16.7 2.6 19.1 6.0 4.6 76.6

Trematomus hansoni 21.1 148.0 77.0 23.0 3.8 16.3 2.8 16.4 5.5 4.2 76.2

Trematomus lepidorhinus 27.4 217.0 71.3 28.7 9.4 15.1 2.5 32.9 7.8 6.1 78.9

Trematomus pennellii 14.1 46.1 78.3 21.7 2.7 15.5 3.3 12.6 4.8 3.6 75.7

Trematomus scotti 12.9 13.4 78.6 21.4 0.5 16.2 4.7 2.4 3.9 2.9 74.3

§ Oftedal, Vecchione, Eisert et al., unpublished data; † ca. 85% of lipids are wax esters (Phleger et al. 1999) with an assumed digestibility of 50% (Place 1991); ‡ ca. 10% of GE is chitin; a) composition data from Clarke (1980) and Pond et al. (1995); b) based on data Friederich & Hagen (1994), CP and ash were estimated by difference and using the CP: ash ratio for P. antarcticum in Lenky et al. (2012)

13

Even if silverfish are consumed in abundance at some times and locations, this is by no means universal.

Note that Fuiman et al. (2002) found in McMurdo Sound that “The relative abundance of Pleuragramma

varied greatly from year to year, as indicated by ‘‘catch per unit effort’’. […] No Pleuragramma were

observed in 1997, 34 were observed in 1998 (all by one seal between 27 and 29 November), and 302 in

1999 (by all five seals)”. Similar observations were made in the Weddell Sea by Plötz et al., who found

that while Weddell seals preyed heavily on silverfish in two of three study seasons at the same site,

silverfish were completely absent from stomach contents and replaced by other prey (primarily

channichthyids) in one year (Plötz 1986; Plötz et al. 1991, 2001).

III.3 Evidence for Toothfish Consumption by Weddell Seals

There is a marked discrepancy between direct evidence for toothfish consumption by Weddell seals –

i.e., observation by underwater cameras, in stomach contents, or by eye witnesses (Murphy 1962;

Dearborn 1965; Calhaem & Christoffel 1969; Ross et al. 1982; Plötz 1986; Davis et al. 1999; Fuiman et al.

2002; Kim et al. 2005; Ponganis & Stockard 2007; Ainley & Siniff 2009) – and conclusions drawn from less

immediate methods for estimating diet (analysis of stable isotopes and scat hard part analysis). Possible

explanations for this discrepancy include:

Weddell seals only feed on toothfish under specific, relatively rare circumstances (such as when

ice holes are prepared by scientists);

preying on toothfish represents a dietary specialisation that is only practiced by a

subpopulation of seals, which is not adequately represented by existing methods (dietary

specialisation was suggested by Ponganis & Stockard 2007);

methods other than direct observation are biased, i.e., likely to underreport or miss toothfish

consumption entirely.

Reports of observed toothfish consumption by Weddell seals describe predation on subadult and adult

toothfish, with an approximate range of 7 to 30 kg body mass and total length of up to 1.3 m (Murphy

1962; Dearborn 1965; Calhaem & Christoffel 1969; Ponganis & Stockard 2007; Hanchet et al. 2008;

Ainley & Siniff 2009). Most observations of toothfish predation by Weddell seals were incidental to an

unrelated research activity (e.g., fish biology, penguin dive physiology) that required drilling and

maintaining large holes in the sea ice, which were subsequently utilised by Weddell seals to catch and

process toothfish. Due to the anecdotal nature of reports, there may be a bias towards reporting the

largest fish caught. For example, Calhaem and Christoffel (1969) give a detailed description of one of the

largest fish taken from a Weddell seal (29.3 kg and 1.25 m total length), but provide fewer details on

smaller specimens. However, it is clear that despite their somewhat specialised dentition (Stirling

1969c), Weddell seals are capable of preying on adult toothfish, although they may not be able to catch

the largest size classes (>1.4 m TL). It is possible, as suggested by Ponganis & Stockard (2007), that

toothfish hunting represents a specialised skill limited to older or more experienced seals (but note that

a large toothfish carcass was defended by a subadult Weddell seal; Kim et al. 2005).

14

Energy content [kJ.g-1 wet mass]

0 1 2 3 4 5 6 7 8 9 10 11

Gymnoscopelus nicholsi

Dissostichus mawsoni muscle

Trematomus lepidorhinus

Gymnoscopelus braueri

Pleuragramma antarcticum 31g

Electrona antarctica

Electrona carlsbergi

Trematomus eulepidotus

Pagothenia borchgrevinki

Trematomus bernacchii

Pleuragramma antarcticum 24g

Trematomus hansoni

Trematomus pennellii

Lepidonotothen squamifrons

Euphausia superba

Trematomus scotti

Bathylagus antarcticus

Pareledone sp. (Octopus)

Pleuragramma antarcticum 8.0g GE

ME

Median ME content

IV. Energy Requirements of Weddell seals in Relation to Prey Nutritional Value

IV.1 Prey Nutritional Value

The nutritional quality of prey is not only essential for estimating biomass intake, it also determines how

predators respond to changes in the availability of particular prey (Moore 2012), and is therefore a key

variable in ecological modelling (Raubenheimer et al. 2009). Nutritional quality of prey is defined by its

proximate composition (lipid, protein, water, carbohydrate, minerals)1 and metabolisable energy

concentration, i.e., the amount of energy that the predator can extract from the food. The total or gross

energy content of food (GE) is equal to the energy released by combustion, i.e., the complete oxidation

of all constituents to CO2, NOx, and water. The utilisation of energy from food is always less than the GE

content and is primarily limited by (1) incomplete digestion (e.g., due to presence of refractory

compounds), (2) the metabolic costs of digestion and assimilation, and (3) loss of energy in urine and

faeces. Subtracting these costs from dietary GE allows the calculation of the energy available to animals

from food, called metabolisable energy (ME).

Figure 3: A comparison of gross (GE) and metabolisable (ME) energy concentration of fish and invertebrate prey. See Table 3 for further details.

This calculation is simplified in fish-eating mammals, as fish is generally highly digestible and the principal

macronutrients are fat and protein, with only traces of carbohydrate (Donnelly et al. 1990; Lenky et al.

1 Predators obviously also require micronutrients such as vitamins and minerals, but no information is available for Antarctic megafauna.

15

2012). Relatively large losses are incurred in the assimilation of protein, which reduce the energy

content of dietary protein from 23.6 kJ.g-1 (GE) to 16.7 kJ.g-1 (ME; Blaxter 1989). There is uncertainty

regarding the digestibility of some compounds found in Antarctic prey, such as chitin (e.g., krill; Clarke

1980) or wax esters (e.g., some myctophids; Phleger et al. 1999), as both are poorly digested by

terrestrial mammals (Place 1992; Mårtensson et al. 1994).

As shown in Figure 3 and Table 3, the ME concentration of fish and invertebrate prey in the Ross Sea

studied to date varies by more than a factor of 4, and ME accounts for less than 75% of GE in low-fat

prey and prey containing a significant proportion of indigestible components (Table 3). It follows that

estimates of predator biomass intake need to take into account prey energy content, as predators have

to eat proportionately more of a lower-quality prey to meet their requirements. In some Antarctic fish,

proximate composition is correlated with age/size, with larger size classes generally lower in water and

higher in lipid and energy (Donnelly et al. 1990), and this applies also to silverfish (Table 3; Wöhrmann et

al. 1997). As a result, the nutritional value of silverfish depends on the age/size class selected by, or

available to, the predator. Together with biomass density, ME content is likely to be the primary factor

determining whether predators can substitute one prey for another (e.g., silverfish vs. toothfish).

IV.2 Estimating Weddell Seal Energy Requirements

While information on Weddell seal energetics is scarce, mammalian metabolism is based on fundamental

concepts that can be applied to estimate Weddell seal energy requirements with a reasonable degree of

confidence. The guiding principle of mammalian energetics is that energy metabolism scales

allometrically with species size. This means that the rate of energy production, or metabolic rate, of

mammals does not increase linearly with BM, but scales to mass raised to the three-quarter power,

BM0.75 (Brody 1945; Kleiber 1975). Hence it is useful to express metabolic rates on a ‘metabolic mass’

basis (Joules per kg BM0.75 per day).

We present estimates for the annual energy budget of different subpopulations of Weddell seals

(breeding females, breeding males, non-breeding adults, and subadults) in Table 4, and a conceptual

model for the annual changes in BM, energy expenditure, and food energy intake of breeding female

Weddell seals (as the subpopulation expected to have the highest overall energy expenditure) in

Figure 4. Younger age classes (BM < 150 kg) are unlikely to prey on toothfish and were not considered in

this analysis. To estimate the annual energy budget of Weddell seals, we used reported data on resting

metabolic rates of Weddell seals in McMurdo Sound, and added in the costs of reproduction, recovery of

mass lost during the breeding season, and the annual moult using published parameters for pinnipeds,

terrestrial mammals, and unpublished data from our own studies on the energetics of lactation in

Weddell seals (Oftedal & Eisert 2010). We assumed a priori that (a) over the course of a year, energy

expenditure would equal food intake, with no net change in body energy, and (b) Weddell seals practice

hyperphagia during the post-breeding period (December-February) and rapidly recover two-thirds of the

body mass lost during the breeding period in the three months after weaning.

Williams et al. (2004) report resting metabolic rates (RMR) of 117.8 kJ.kg-1 BM for adult Weddell seals

with a mean BM of 387.4 kg, equivalent to 0.523 MJ.kg-0.75.day-1. We multiplied the RMR by a factor of

1.5 to arrive at an estimate for the field metabolic rate (FMR) for adult Weddell seals at maintenance of

0.784 MJ.kg-0.75.day-1 (Sparling et al. 2008). This FMR estimate was used to estimate maintenance

metabolism from body mass (i.e., metabolic expenditure without any added costs such as gestation,

moult, or mass recovery) for seals that were not lactating. For energy expenditure during the lactation

16

period, we determined mean values of 0.576, 0.522 and 1.56 MJ.kg-0.75.day-1 in Weddell seals during

early, mid-, and late lactation using the double-labelled water method (Eisert, Oftedal, Michener,

unpublished data; Sparling et al. 2008).

The cost of gestation was estimated by assuming that the GE content of the neonate (30 kg, 6.84 MJ.kg-1;

Eisert, Oftedal, Hood, Mitchell, unpubl. data) accounted for 82% of the energy content of the conceptus

(term foetus plus placenta, uterus, and associated structures), as is the case in terrestrial ungulates with

single offspring of similar maturity at birth as Weddell seals (Oftedal 1985; Eisert et al. 2013b). The

efficiency of energy retention of the conceptus was assumed to be 13.3% (Oftedal 1985). Foetal growth

in Weddell seals was modelled using unpublished data from Weddell seals in Smith (1966), assuming that

foetal growth followed the same general pattern as in the harp seal Pagophilus groenlandicus (Yunker et

al. 2005).

The energy cost of lactation was estimated by multiplying an average milk yield of 3.54 kg.d-1 in Weddell

seals (Tedman & Green 1987) with measured GE content of Weddell seal milk (Eisert et al. 2013a) and a

lactation period of 42 days. No allowance was made for the costs of milk synthesis, as we measured

oxidative metabolism during the lactation period and this already includes the energy expended for milk

synthesis (as opposed to the energy content of the milk produced).

Mass loss of breeding females (Eisert & Oftedal 2009) and males (Bartsh et al. 1992) was estimated from

published values. The cost of recovery for lost mass was calculated by assuming a ratio of fat to lean

mass gain of 1: 1 and a growth efficiency of 70% (Blaxter 1989; Eisert 2003; Oftedal & Eisert 2010). For

the construction of the annual model of energy expenditure in breeding females (Fig. 4), it was assumed

that seals would regain mass at a rate sufficient to achieve 85% of their postpartum BM within three

months of weaning, and recover the remaining body weight slowly between March and October.

To simplify model calculations, we assumed that BM of adult seals would stay constant from year to

year, which is not strictly true as adult Weddell seals continue to grow at a slow rate (Bryden et al. 1984).

For subadult seals, we assumed a mean BM of 150 kg, an FMR of 0.586 MJ.kg-0.75.day-1, and a growth rate

of 50 kg per year (Bryden et al. 1984; Boily & Lavigne 1995), using the same parameters for estimating

cost of growth as for recovery of lost mass in adult seals (above).

To estimate the cost of the moult, an increment of on average 15% was added to the estimated RMR for

a period of 30 days based on findings in captive grey seals, Halichoerus grypus (Boily 1996). Like grey

seals and unlike many other pinnipeds, Weddell seals do not fast during the moult (Smith 1966).

An interesting outcome of the analysis presented here is that the energy costs of reproduction

significantly elevate the mean annual energy expenditure relative to non-breeding seals (based on FMR),

by a factor 1.44 and 1.13 in breeding females and males, respectively (Table 4). Secondly, peak energy

expenditures of Weddell seals during certain periods are predicted to be very high, for example during

the late lactation period (100 – 200 MJ.day-1), and presumably also during the post-breeding recovery

(note that this is driven by the assumption of rapid mass recovery post-breeding). Weddell seals not only

lose a lot of mass during the breeding season, they lose lean mass and body fat in approximately equal

proportions (Eisert 2003; Oftedal & Eisert 2010). The efficiency of regaining lost lean mass is poor (≤0.7),

and hence mass recovery requires significant overfeeding (hyperphagia). We have no information over

what time scale lost mass is recovered after the end of the breeding season; it was assumed as a first

approximation that seals regain ca. two-thirds of the lost mass during the first three months after the

end of lactation, and regain the remaining mass slowly until parturition the following year. This was

based on the assumption that food will be more abundant during the summer months. Obviously, the

daily rate of energy expenditure and the shape of the food intake curve shown in Fig. 4 will depend on

17

rate of mass gain and the timing of when hyperphagia takes place, but assumed timing does not affect

the estimate of the overall annual expenditure. The assumption that Weddell seals practice post-

breeding hyperphagia is supported by the observations of Calhaem & Christoffel (1969), who reported

that one Weddell seal caught four toothfish with a combined weight of 54 kg within 24 hours on

December 10, 1966, and kept up high rates of toothfish consumption during the entire 14-day

observation period (the authors estimated that the average daily toothfish catch was ca. 68 kg).

Assuming a dress-out rate of 60% (Ainley & Siniff 2009), 54 kg of whole toothfish equates to an intake of

ca. 32.4 kg and 275 MJ of energy (ME), vastly in excess of the estimated daily FMR for adult seals of

66 MJ.d-1 (Table 4) but similar to peak rates of ME intake predicted by the model shown in Fig. 4. While

it has been reported that Weddell seals cache toothfish in crevices in the sea ice (Kim et al. 2005;

Ponganis & Stockard 2007), Calhaem & Christoffel (1969) specifically stated that the seal ate the

toothfish it caught, starting with the viscera. Both immediate consumption of toothfish and caching

behaviour by Weddell seals are described by Ponganis & Stockard (2007). A fish biologist reported that

he once recovered a toothfish from which a seal had removed only the viscera but left most of the dorsal

musculature intact (Prof. William Davison, pers. comm.).

Observations of both prey caching and possibly selective consumption indicate that at least some

Weddell seals some of the time are faced with an overabundance of toothfish, based on analogous

behaviour in terrestrial carnivorans such as felids (Leyhausen 1979). As pointed out by Ainley & Siniff

(2009), prey caching and defence indicate that toothfish are ‘valuable’ to Weddell seals. Large predators

such as tigers and leopards will also return to and defend prey carcasses that are too large to be

consumed at once (Dr. John Seidensticker, pers. comm.).

18

Table 4: Annual energy budget for different subpopulations of Weddell seals, including the ratio of field metabolic rate (FMR) and overall expenditure. A

conceptual model of the annual variation in energy expenditure for breeding female Weddell seals is shown in Fig. 4. Please see text for details of the

calculation.

BM FMR mass loss growth growth gestation lactation moult annual total annual ratio

Seal category [kg] [MJ.day-1] [kg] [kg.y-1] [MJ] [MJ] [MJ] [MJ] [GJ.y-1]

total expenditure/

total FMR

adult female, breeding 394 70.3 188 188 6,055 1,809 3,068 244 36.8 1.44

adult male, breeding 360 63.6 88 88 2,796 -- -- 191 26.2 1.13

non-breeding adult 371 65.6 0 0 - -- -- 197 24.1 1.01

subadult 150 37.7 0 50 1,597 -- -- 113 15.5 1.12

19

Figure 4: A conceptual model of the seasonal variation in body mass, food intake (as metabolisable energy, ME), and daily energy expenditure of an adult female Weddell seal. All three variables were measured only during the lactation period (Eisert, Oftedal, Michener, et al. unpubl. data). The model includes the energy costs of maintenance, gestation, lactation, moult, and recovery of mass lost during lactation. It was assumed a priori that (a) over the course of a year, energy expenditure would equal food intake, with no net change in body energy, and (b) Weddell seals practice hyperphagia during the post-breeding period (December-February) and rapidly recover two-thirds of the body mass lost during the breeding period in the three months after weaning. Total annual energy expenditure is ca. 36.8 GJ.y-1, equivalent to a daily average expenditure of 101 MJ.d-1 (see also Table 4). Further sources and assumptions are explained in the text. EB, embryonic diapause; F, fertilisation; I, implantation; P, parturition; W, weaning.

20

IV.3 Comparison of Weddell Seal Energy Requirements with Prey Energy Content

We combined information on the energy content of prey (section IV.1) with estimated energy

expenditure of adult Weddell seals (section IV.2) to determine the amounts of prey required per day by

Weddell seals in two different states, at maintenance (FMR) and relative to the mean annual daily

expenditure of a breeding female, as the subgroup expected to have the highest energy expenditure

(Table 3). We calculated requirements for three types of prey that are purportedly consumed by

Weddell seals, juvenile silverfish, adult silverfish, and toothfish, and plotted the results both in terms of

prey biomass (kg per day, Fig. 5A) and number of individual prey items (number per day, Fig. 5B).

The ME concentration of the three prey types differs by a factor of four, from 2.2 kJ.g-1 wet mass in

juvenile silverfish to 8.6 kJ.g-1 wet mass in toothfish muscle (Table 3), and biomass requirements of

Weddell seals are predicted to vary linearly with prey ME content (Fig. 5A). It should be noted that the

maximum recorded stomach fill for Weddell seals is 17 kg (Plötz 1986), which does not mean that daily

consumption cannot exceed this amount, but it provides an approximate reference point. Weddell seals

may be physically unable to consume sufficient prey with a low ME content to meet their energy

requirements. Weddell seal foraging behaviour in McMurdo Sound and elsewhere follows a diurnal or

quasi-diurnal pattern (Smith 1965; Siniff et al. 1971; Bornemann et al. 1998), with one broad peak of

foraging activity per 24-hour period. This suggests that Weddell seals fill their stomach and then haul

out to digest their prey. Transit time from ingestion to defaecation or defaecation frequency are not

known for Weddell seals. Reported transit times for fish prey in harp and leopard seals are

approximately 8 to 17 hours and 18 to 25 hours, respectively (Mårtensson et al. 1998; Hall-Aspland et al.

2011).

An important factor affecting the feasibility of meeting feeding requirements is the size of individual prey

items and the degree of clustering of the prey – toothfish are both very large and energy-rich and thus

represent a highly clustered resource (Mangel & Adler 1994). Silverfish are small-bodied but occur in

shoals, so that their energy density depends on abundance and shoal density in addition to size class.

Camera systems lowered through the water column from research vessels (J.T. Eastman, pers. obs.), and

‘critter cams’ deployed on Weddell seals (Fuiman et al. 2002) indicate Antarctic silverfish exist as loose

shoals (unstructured aggregations), with individuals estimated to be spaced 2–4 m apart at densities of

one fish per 7–43 m3 (Fuiman et al. 2002; La Mesa & Eastman 2012). Multi-frequency acoustic estimates

of silverfish density in the Ross Sea (O'Driscoll et al. 2011) indicate maximum silverfish densities of one

fish per 5 m3 (back-scattering strength recordings SV of -70 dB; R. O’Driscoll, pers. comm.). Due to the

small size and low ME content of juvenile silverfish, an implausible large number (~4,000 fish per day)

would be required to meet Weddell seal daily energy expenditures. Burns & Kooyman (2001) have

suggested that Weddell seals and emperor penguins both feed primarily on juvenile silverfish of ≤ 10 cm

SL (i.e., with an individual BM of ca. 5-10 g), but energetic considerations indicate that this is unlikely for

Weddell seals. By contrast, large, more lipid-rich adult silverfish (≥30 g, SL 15-16 cm) can be taken by

Weddell seals in numbers adequate for meeting daily requirements (Fig. 5B; Plötz 1986: “The number of

P. antarcticum taken by the individual seals ranged between 139 and 508.”).

Given the strong positive correlation between silverfish age/size and energy content, it is interesting to

note that direct evidence from stomach sampling (Plötz 1986; Green & Burton 1987; Plötz et al. 2001)

and underwater cameras (Fuiman et al. 2002) indicates that Weddell seals consume a larger size range of

silverfish (mean reported SL 15 to 20 cm, equivalent to BM of 25 to 65 g) than the size range calculated

indirectly from otoliths recovered in seal faeces (mean reported SL 10 to 14 cm, equivalent to BM of 7 to

21 g; Castellini et al. 1992; Burns et al. 1998; Burns & Kooyman 2001; O'Driscoll et al. 2011).

21

Figure 5: Amount (A) and numbers (B) of toothfish and two different size classes of silverfish (8 and 31 g body mass; see Table 2) required to meet mean daily average energy expenditures for an adult Weddell seal at maintenance and for a breeding female Weddell seal (annual average; refer Table 4).

A. Biomass

prey type

silverfish (juvenile) silverfish (adult) toothfish

kg r

equi

red

per

day

0

10

20

30

40

adult at maintenance

breeding female, mean annual expenditure [MJ.day-1]

maximum observed stomach fill (Plötz et al. 1986)

B. Prey numbers

prey type

silverfish (juvenile) silverfish (adult) toothfish

indi

vidu

al p

rey

item

s re

quir

ed p

er d

ay

0

100

200

300

400

4000

5000

6000adult at maintenance

breeding female, mean annual expenditure [MJ.day-1]

n = 1.1

n = 0.7

22

This suggests that the silverfish size preferred by Weddell seals may have been underestimated due to a

failure to adequately compensate for otolith erosion during digestion (Grellier & Hammond 2006). While

seals are likely to consume all silverfish available and hence ingest a range of fish sizes (Plötz et al. 2001),

larger fish will make a greater contribution in terms of biomass and ME.

In summary, it appears that large, high-fat silverfish occurring at relatively high densities that allow a

daily ingestion of 200-500 fish (i.e., a high rate of catch per unit effort in terms of ingested energy)

represent a feasible nutritional resource for Weddell seals, and may be preferred by seals. On the other

hand, it is unlikely that Weddell seals can meet their energy needs feeding on smaller silverfish or

silverfish occurring at low densities, in particular during periods of high energy demand. This proposition

is in good agreement with the observation (see section III.2) that the contribution of silverfish to Weddell

seal diets is highly variable and that seals readily switch to other prey when silverfish abundance is low

(Plötz et al. 1991; Fuiman et al. 2002).

V. Weddell Seal Abundance Estimates

In contrast to extensive demographic information available for the Erebus Bay/eastern McMurdo Sound

region, abundance estimates for the Ross Sea are based on aerial surveys from the late 1960s (Stirling

1969a) and urgently require revision. This represents a significant knowledge gap, because accurate

estimates of Weddell seal abundance for the Ross Sea are required to estimate total prey biomass

consumption and the plausible proportion of toothfish in Weddell seal diets (based on the comparison of

toothfish mortality with seal biomass consumption; see below). In the absence of more spatially

comprehensive population monitoring, it is also currently not possible to detect whether populations are

changing in response to external factors.

Estimating seal abundance from satellite observation has recently been developed as an option (LaRue et

al. 2011) but to be accurate, this method requires extensive ground-truthing and better information on

seal diurnal activity patterns, as seals diving below the ice will not be seen. Accuracy of satellite surveys

was particularly poor (recovery <50 %) for aggregations of fewer than 200 seals relative to ground

surveys (LaRue et al. 2011), suggesting that a significant proportion of the population may be missed.

While Weddell seals are the only pinniped breeding in the Ross Sea, hence all seal colonies can be

assumed to consist of Weddell seals, satellites may fail to detect parts of the population not present in

breeding colonies. In McMurdo Sound, seals in breeding colonies represent approximately 70% of the

total population (Stirling 1969b). Breeding males defend underwater territories (maritories) and their

visibility may therefore be reduced until after the mating season (Harcourt et al. 2007). Satellite surveys

probably cannot distinguish between different seal species in the pack ice. Since it is likely that subadult

Weddell seals disperse into the pack ice, surveys of breeding colonies are a necessary, though perhaps

not sufficient, requirement for obtaining accurate information on Weddell seal abundance in the Ross

Sea region.

VI. Comparison of Estimates of Toothfish Mortality and Weddell Seal Consumption in the McMurdo

Sound region

A spatially explicit estimate of toothfish biomass and mortality was derived in Pinkerton et al. (2008) and

used to estimate a plausible upper bound on toothfish biomass of 4,400-7,770 t in the region bounded to

the North by 76°S and to the east by 175°E. Scientific tagging/recapture rates were used to give an early

estimate of the biomass of Antarctic toothfish in the McMurdo Sound region of 2,700 t (Raymond 1975),

23

which is of a similar order of magnitude. Toothfish natural mortality has been taken as M = 0.13 y-1

(Dunn et al. 2006). Assuming that annual mortality scales with biomass, estimated toothfish mortality in

the defined region is equivalent to ca. 950 t. The majority of this mass of fish are assumed to be

consumed by predators. The most likely predators in the McMurdo Sound region are Weddell seals and

Type C killer whales. It is possible that most of the annual predation on toothfish in this region occurs

between November and February, when the largest number of Weddell seals are present (Smith 1965),

toothfish appear higher in the water column (Ainley et al. 2012), and seals have access to a greater

portion of the sound due to break-up of the sea ice (Stirling 1969b).

Currently available data on stable isotope enrichments in Weddell seals and their prey are consistent

with a dietary contribution of toothfish of 15% (Table 1), although this estimate should be considered

provisional as discussed in section III.1. Assuming that toothfish represents 15% of the total annual

energy intake of all subpopulations listed in Table 4, the estimated total consumption of toothfish by

Weddell seals, calculated from the ME content shown in Table 3, is 2,128 t.yr-1. If consumption of

toothfish is assumed to be restricted to the months of November, December, and January (i.e., Weddell

seal energy expenditure includes 3 months of FMR, plus the costs of reproduction and of 50% of the

mass recovery), the total consumption estimate is 626 t of toothfish. This estimate is lower than

estimated toothfish mortality. If 100% of toothfish natural mortality in this region is assumed to arise

from Weddell seal predation in summer (i.e., no mortality during the other 9 months of the year and no

predation by Type C killer whales), then a diet composition of up to 22% toothfish (= 918 t) for the period

November to January would be consistent with estimated toothfish biomass and mortality. It has been

suggested that successful toothfish hunting may represent a dietary specialisation in Weddell seals and

may be restricted to older, larger, or more experienced seals (Ponganis & Stockard 2007). If this the

case, then individual seals or subpopulations may have a significantly higher intake of toothfish than

estimated here, but this is speculative in the absence of further research.

SUMMARY

Nutritional analysis of Ross Sea prey suggests that toothfish may represent a unique high-energy food

resource for Weddell seals that possibly cannot be adequately replaced by other prey, in particular

during periods of high energy demand such late-stage lactation and the post-breeding recovery of body

weight and condition. The assumed dominance of silverfish in Weddell seal diets should be re-examined

given the known biases of methods used to derive diet estimates. While large (>30 g) silverfish occurring

at high densities are a valuable nutritional resource, smaller size classes are unlikely to be adequate to

meet the estimated energy expenditures of adult Weddell seals, in particular during periods of high

energy demand. Preliminary calculations based on energetic considerations and estimated population

sizes of both toothfish and Weddell seals in the McMurdo Sound region suggest that toothfish may be a

minor (up to 20%) but potentially critical component of Weddell seal diet in this area. Our ability to

conclusively determine possible dependence of Weddell seal populations on toothfish, and hence

possible impacts of toothfish removal by fisheries, is primarily hindered by (a) insufficient information on

diet, due to inadequate temporal coverage and biased methodology, and (b) uncertainty regarding

Weddell seal abundance in the Ross Sea.

24

RECOMMENDATIONS

we urgently need better information on diet of Weddell seals, specifically (a) during periods not

currently covered and (b) utilising methodology that can conclusively detect toothfish

consumption

we need updated Weddell seal abundance estimates for the Ross Sea; satellite surveillance may be

an option, but needs to be complemented by extensive ground-truthing to ensure accuracy

we require refined estimates of energy requirements of Weddell seals, in particular during the

post-breeding season

we need improved understanding of spatial habitat utilisation and foraging behaviour, especially in

the post-moult period and during winter

accurate estimation of predator requirements would benefit greatly from a comprehensive prey

database for the Ross Sea that includes information on GE content, ME content, proximate

composition, and information on non-standard constituents (wax esters, chitin)

we need to take into account other potential predators of toothfish (killer whales, leopard seals)

Acknowledgements

This work was part-funded by the New Zealand MBIE project C01X1001 (“Protecting Ross Sea Ecosystems”) and by Gateway Antarctica, University of Canterbury, Christchurch. Field studies on Weddell seals were supported by a grant from the National Science Foundation-Office of Polar Programs ANT-0538592 to OTO, RE and D. Boness. Members of the New Zealand Antarctic Fisheries Working Group provided useful comments on an earlier draft of this paper.

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